anger and aggression: human functional neuroimaging and...

Anger: A review of human electrophysiology 1

Anger: A review of human electrophysiology and functional neuroimaging research

Eddie Harmon-Jones

University of Wisconsin – Madison

Address correspondence to:

Eddie Harmon-Jones University of Wisconsin--Madison Department of Psychology 1202 West Johnson Street Madison, Wisconsin 53706-1611 phone: (608) 265-5504 fax: (608) 262-4029 email: [email protected]


Evidence from a variety of research approaches has pointed to the importance of

asymmetrical frontal cortical activity in emotional/motivational processes. Much of this

evidence has been obtained with electroencephalographic (EEG) measures of brain

activity, or more specifically, alpha frequency band activity derived from the EEG.

Research has revealed that alpha power is inversely related to regional brain activity

using hemodynamic measures (Cook, O’Hara, Uijtdehaage, Mandelkern, & Leuchter,

1998) and behavioral tasks (Davidson, Chapman, Chapman, & Henriques, 1990).

Additional data from individuals with brain damage supports the research with EEG (e.g.,

Robinson & Downhill, 1995).

In the EEG research, depression has been found to relate to resting frontal

asymmetrical activity, with depressed individuals showing relatively less left than right

frontal brain activity (Jacobs & Snyder, 1996; Schaffer, Davidson, & Saron, 1983).

Moreover, relatively less left frontal activity has been found in individuals who were

previously clinically depressed but were in remission status (Henriques & Davidson,

1990).

Other research has revealed that trait positive affect is associated with greater left

than right frontal brain activity, whereas trait negative affect is associated with greater

right than left frontal brain activity (e.g., Tomarken, Davidson, Wheeler, & Doss, 1992).

Still other research has found that trait behavioral activation sensitivity (BAS) relates to

greater left than right frontal brain activity (Harmon-Jones & Allen, 1997; Sutton &

Davidson, 1997).


In addition to the research that suggests that resting baseline frontal asymmetrical

activity relates to other measures of trait emotion and motivation, research has found that

resting baseline frontal asymmetrical activity predicts emotional responses. For example,

individuals with relatively greater right than left frontal activity during baseline recording

sessions report larger negative affective responses to negative emotion-inducing films

(fear and disgust) and smaller positive affective responses to positive emotion-inducing

films (happiness) (Tomarken, Davidson, & Henriques, 1990; Wheeler, Davidson, &

Tomarken, 1993). Moreover, relative right frontal activity at baseline predicts crying in

response to maternal separation in 10-month-old infants (Davidson & Fox, 1989).

Research has also demonstrated that asymmetrical frontal brain activity is

associated with state emotional responses. For instance, Davidson and Fox (1982) found

that 10-month-old infants exhibited increased left frontal activation in response to a film

clip of an actress generating a happy facial expression as compared to a sad facial

expression. Frontal brain activity has been found to relate to facial expressions of positive

and negative emotions, as well. For example, Ekman and Davidson (1993) found

increased left frontal activation during voluntary facial expressions of smiles of

enjoyment. More recently, Coan, Allen, and Harmon-Jones (2001) found that voluntary

facial expressions of fear produced relatively less left frontal activity.

Finally, biofeedback training has been used to manipulate asymmetrical frontal

cortical activity and the effects of this manipulation on emotional responses have been

observed (Allen, Harmon-Jones, & Cavender, 2001). These results suggest that the

frontal asymmetry can be altered using biofeedback training and that this alteration can

affect emotional responses, with an increase in left frontal cortical activity causing more


happy emotional facial expressions and an increase in relative right frontal cortical

activity causing more sad emotional facial expressions. Taken together, this research

suggests that asymmetrical frontal cortical activity is causally involved in emotional

responses (for a more detailed review, see Coan & Allen, 2003).

Explanations of the Relationship between Asymmetrical Frontal Activity and

Emotion/Motivation

All of this past evidence can be summarized within one of three theoretical

models. According to the valence model, the left frontal brain region is involved in the

experience and expression of positive emotion and the right frontal brain region is

involved in the expression and experience of negative emotion (e.g., Ahern & Schwartz,

1985; Gotlib, Ranganath, & Rosenfeld, 1998; Heller, 1990; Heller & Nitschke, 1998;

Silberman & Weingartner, 1986). Indeed, research is consistent with this model and it is

widely accepted (e.g., Oatley & Jenkins, 1996; Zajonc & McIntosh, 1992).

According to the motivational direction model, the left frontal brain region is

involved in expression of approach-related emotions and the right frontal brain region is

involved in expression withdrawal-related emotions (Fox, 1991; Harmon-Jones & Allen,

1997; Sutton & Davidson, 1997). Again, the obtained results can be accommodated by

this model. That is, the affects and emotions that have been examined in the research are

all associated with approach or withdrawal motivation. The approach-related emotions

have been found to be associated with relatively greater left frontal activity, whereas the

withdrawal-related emotions have been found to be associated with relatively greater

right frontal activity.


According to the valenced motivation model, the left frontal brain region is

involved in the expression and experience of positive, approach-related emotions and the

right frontal brain region is involved in the expression and experience of negative,

withdrawal-related emotions (Davidson, 1998; Tomarken & Keener, 1998). The obtained

results can also be accommodated by this model. That is, the positive affects that have

been examined in the research are all associated with approach motivation, and the

negative affects that have been examined are all associated with withdrawal motivation.

Because the previously conducted research confounded the valence of the

emotion with the direction of motivation, it had been unable to address whether the

frontal asymmetry reflects the valence of the emotion, the direction of the motivation, or

a combination of valence and motivation. Often, positive emotion is associated with

approach-related motivation, whereas negative emotion is associated with withdrawal-

related motivation. Indeed, most contemporary theories of emotion posit that positive

emotion is always associated with approach motivation and that negative emotion is

always associated with negative emotion (Gray, 1994a, 1994b; Watson, 2000; for a

different point of view, see Carver, 2001). However, not all emotions behave in accord

with this assumed relationship between the valence of emotion and direction of

motivation. Anger is one of the best examples of a violation of the relationship, because

anger is negative in valence (e.g., Lazarus, 1991; Watson, 2000), but it often evokes

approach motivation (e.g., Berkowitz, 1999; Darwin, 1872/1965; Plutchik, 1980; Young,

1943).

In addressing the exact emotional/motivation functions of asymmetrical frontal

brain activity, my colleagues and I have examined the emotion of anger, as it is a


negative emotion that often evokes approach motivational tendencies. In support of the

motivational direction model over the other two models, recent evidence has suggested

that anger and aggression may be associated with greater left than right frontal cortical

activity. In this chapter, I will review the evidence supportive of such a relationship.

Then, I will briefly consider evidence, seemingly inconsistent with the aforementioned

research, that suggests that aggression is associated with decreased frontal cortical

activity. In the end, I will offer some resolutions to these apparent discrepancies and

suggest some further empirical tests of the relationship between anger, aggression, and

frontal cortical activity.

Anger and Approach Motivation

Before reviewing the research on anger and asymmetrical frontal activity, it is

important to consider whether anger is associated with approach motivation. Several lines

of research suggest that anger elicits behavioral approach or approach motivation

tendencies.

Behavioral Evidence

In the animal behavior literature, a distinction has been made between offensive

or irritable aggression and defensive aggression (Flynn, Vanegas, Foote, & Edwards,

1970; Moyer, 1976). It has been posited that irritable aggression results from anger and

that pure irritable aggression “involves attack without attempts to escape from the object

being attacked” (Moyer, 1976, p. 187). A number of aggression researchers have

suggested that offensive aggression is associated with anger, attack, and no attempts to

escape, whereas defensive aggression is associated with fear, attempts to escape, and

attack only if escape is impossible (Blanchard & Blanchard, 1984; Lagerspetz, 1969;


Moyer, 1976). In demonstrating that organisms evidence offensive aggression and that

this is an approach behavior, Lagerspetz (1969) found that under certain conditions mice

would cross an electrified grid to attack another mouse.

With adult humans, Baron (1977) demonstrated that signs of their tormentor’s

pain reinforce angry persons positively. The participants who had been deliberately

provoked by another individual then had a sanctioned opportunity to assault him.

Indications that their first attacks were hurting their target led to intensified aggression

even though the unprovoked participants reduced the intensity of their punishment at

learning of the other’s pain. The initial signs of their victim’s suffering showed the angry

persons they were approaching their aggressive goal and evoked even stronger assaults

from them (see also, Berkowitz, Cochran, & Embree, 1981).

Subsequent to frustrating events, anger may maintain and increase task

engagement and approach motivation. Lewis, Sullivan, Ramsay, and Alessandri (1992)

found that infants who expressed anger during extinction maintained interest during

subsequent relearning, whereas infants who expressed sadness during extinction

evidenced decreased interest during relearning.

Subjective Evidence

Additional support for the idea that anger is associated with approach motivation

comes from research testing the conceptual model that integrated reactance theory with

learned helplessness theory (Wortman & Brehm, 1975). According to this model, how

individuals respond to uncontrollable outcomes depends on their expectation of being

able to control the outcome and the importance of the outcome. When an individual

expects to be able to control outcomes that are important, and those outcomes are found


to be uncontrollable, psychological reactance should be aroused. Thus, for individuals

who initially expect control, the first few bouts of uncontrollable outcomes should arouse

reactance, a motivational state aimed at restoring control. After several exposures to

uncontrollable outcomes, these individuals should become convinced that they cannot

control the outcomes and should show decreased motivation (i.e., learned helplessness).

In other words, reactance will precede helplessness for individuals who initially expect

control. In one study testing this model, individuals who exhibited angry feelings (a

manifestation of reactance) in response to one unsolvable problem had better

performance and more approach motivation on a subsequent cognitive task than did

participants who exhibited less anger (Mikulincer, 1988).

Other research has revealed that state anger relates to high levels of self-

assurance, physical strength, and bravery (Izard, 1991), inclinations associated with

approach motivation. Additionally, Lerner and Keltner (2001) found that anger (both trait

and state) is associated with optimistic expectations, whereas fear is associated with

pessimistic expectations. Moreover, happiness was associated with optimism, making

anger and happiness appear more similar to each other in their relationship with optimism

than fear and anger. Although Lerner and Keltner (2001) interpreted their findings as

being due to the appraisals associated with anger, it seems equally plausible that it was

the approach motivational character of anger that caused the relationship of anger and

optimism. That is, anger creates optimism because anger engages the approach

motivational system and produces greater optimistic expectations.

Hormonal and Physiological Evidence


Further evidence supporting the conceptualization of anger as involving approach

and not withdrawal comes from research on testosterone, which has been found to be

associated with anger and aggression in humans (e.g., Olweus, 1986). In this research,

testosterone treatments have been found to decrease withdrawal (fear) responses in a

number of species (e.g., Boissy & Bouissou, 1994; Vandenheede & Bouissou, 1993).

Other research has demonstrated that damage to the amygdala, a brain region involved in

defensive behavior, has no effect on offensive aggression but reduces reactivity to

nonpainful threat stimuli (Blanchard & Takahashi, 1988; Busch & Barfield, 1974).

Individual Differences Evidence

Other evidence supporting the idea that anger is associated with an approach-

orientation comes from research on bipolar disorder. The emotions of euphoria and anger

often occur during manic phases of bipolar disorder (Cassidy, Forest, Murry, & Carroll,

1998; Depue & Iacono, 1989; Tyrer & Shopsin, 1982). Both euphoria and anger may be

approach-oriented processes, and a dysregulated or hyperactive approach system may

underlie mania (Depue & Iacono, 1989; Fowles, 1993). Research suggests that

hypomania/mania involves increased left frontal brain activity and approach motivational

tendencies. In this research, it has been found that individuals who have suffered damage

to the right frontal cortex are more likely to evidence mania (see review by Robinson &

Downhill, 1995). Thus, this research is consistent with the view that mania may be

associated with increased left frontal activity and increased approach tendencies, because

the approach motivation functions of the left frontal cortex are released and not restrained

by the withdrawal system in the right frontal cortex. Furthermore, lithium carbonate, a

treatment for bipolar disorder, reduces aggression (Malone, Delaney, Luebbert, Cater, &


Campbell, 2000), suggesting that anger and aggression correlate with the other symptoms

of bipolar disorder. In addition, trait anger has been found to relate to high levels of

assertiveness and competitiveness (Buss & Perry, 1992). Finally, trait anger, as measured

by the Buss and Perry (1992) anger subscale, has been found to relate to trait BAS, as

measured by Carver and White’s (1994) questionnaire (Harmon-Jones, in press-a).

While individuals with relatively low left frontal activation are at risk for deficits

in approach motivation and depression, those with relatively high left frontal activation

may evidence excessive approach motivation, leading to increased anger and aggression.

Asymmetrical Frontal Activity and Trait Anger

In all past research on the frontal asymmetry, the valence of the affective style

(positive vs. negative) was confounded with the direction of the motivation (approach vs.

withdrawal). Consequently, scientists have concluded that that the frontal asymmetry

reflects differences in emotional valence (e.g., Ahern & Schwartz, 1985; Gotlib,

Ranganath, & Rosenfeld, 1998; Heller, 1990; Heller & Nitschke, 1998). To address this

confound, Harmon-Jones and Allen (1998) assessed the relationship between resting

frontal asymmetrical activity and anger, an emotion that is negatively valenced but

approach-related. Results indicated that trait anger related to increased left frontal activity

and decreased right frontal activity.

More recently, Harmon-Jones (in press-b) addressed an alternative explanation for

the results of Harmon-Jones and Allen (1998). The alternative explanation suggested that

persons with high levels of trait anger might experience anger as a positive emotion, and

this positive feeling or attitude toward anger could be responsible for anger being

associated with relative left frontal activity. Anger might have been regarded positively


because of the subjective feel or evaluation of the emotion. After conducting three studies

that developed a valid and reliable assessment of attitude toward anger, a study was

conducted to assess whether resting baseline asymmetrical activity related to trait anger

and attitude toward anger. Results indicated that anger related to relative left frontal

activity and not attitude toward anger. Moreover, further analyses revealed that the

relationship between trait anger and left frontal activity was not due to anger being

associated with a positive attitude toward anger.

Asymmetrical Frontal Activity and State Anger

Although the Harmon-Jones and Allen (1998) and the Harmon-Jones (in press-b)

studies suggest that anger is related to relative left frontal activity, both studies are

correlational and subject to the interpretational limitations associated with correlational

studies (e.g., a third variable causes the observed relationship). To address these

limitations, experiments have been conducted in which anger is manipulated and its

effects on regional brain activity are examined.

State Anger Induced via Interpersonal Insult and Asymmetrical Frontal Activity

Harmon-Jones and Sigelman (2001) conducted an experiment to assess whether

situationally induced anger would increase relative left frontal activity. Participants were

randomly assigned to a condition in which another person insulted them or to a condition

in which another person treated them in a neutral manner. Immediately following the

treatment, EEG was collected. As predicted, individuals who were insulted evidenced

greater relative left frontal activity than individuals who were not insulted. Additional

analyses revealed that within the insult condition, reported anger and aggression were

positively correlated with relative left frontal activity. Neither of these correlations was


significant in the no-insult condition. These results suggest that relative left-frontal

activation was associated with more anger and aggression in the condition in which anger

was evoked. This research thus provides the first demonstration of a relationship between

state anger and relative left frontal activation, a result predicted by models that posit that

the frontal asymmetry reflects motivational direction but not predicted by models that

posit that the frontal asymmetry reflects emotional valence.

The Effect of Coping Potential on Anger-Related Left Frontal Cortical Activity

In the experiments reviewed thus far, it was assumed that anger related to left

frontal cortical activity because anger was associated with approach motivation. In

Harmon-Jones and Sigelman (2001), the experiment was designed in a manner to evoke

anger that was approach oriented. Although most instances of anger involve approach

inclinations, not all forms of anger are associated with approach motivation. To

manipulate approach motivation independently of anger, Harmon-Jones, Sigelman,

Bohlig, and Harmon-Jones (2003) performed an experiment in which the ability to cope

with the anger-producing event was manipulated. Based on past research that has

revealed that coping potential affects motivational intensity (Brehm & Self, 1996), it was

predicted that the expectation of being able to take action to resolve the anger-producing

event would increase approach motivational intensity relative to expecting to be unable to

take action.

In the experiment, university students opposed to a tuition increase were exposed

to an editorial that argued for a tuition increase. They were exposed to this

counterattitudinal message, as a large body of research has suggested that exposure to

such messages evokes negative affect (for a review, see Harmon-Jones, 2000).


Conditions differed with regard as to whether it was possible for participants to act to

change the likelihood that tuition will be increased, to manipulate coping potential or the

expectation of acting to change the situation. In the action-possible condition, participants

were told that the increase may occur in the future and that petitions were being

circulated to attempt to prevent the increase. In the action-impossible condition,

participants were told that the tuition increase would definitely occur.

Both conditions evoked significant increases in anger (over baseline) and they

were not significantly different from each other. More importantly and consistent with

predictions, results indicated that participants who expected to engage in the approach-

related action of signing a petition to ameliorate the tuition-increase situation (action-

possible condition) evidenced greater left frontal activity than participants who expected

to be unable to engage in approach-related action. Moreover, within the action-possible

condition, participants who evidenced greater left frontal activity in response to the

tuition increase message also evidenced greater self-reported anger, providing support for

the idea that anger is often an approach-related emotional response. In the condition

where action was not possible, greater left frontal activity did not relate to greater anger.

This is because, although anger usually leads to approach motivation, when action is not

possible, approach motivation should remain low, even if angry feelings are high. Finally,

within the action-possible condition, participants who evidenced greater left frontal

activity in response to the tuition increase message were more likely to engage in

behaviors that would reduce the possibility of the tuition increase (i.e., they were more

likely to sign the petition and to take petitions with them for others to sign). This finding


suggests that greater approach motivation, as reflected in greater left frontal cortical

activity, was associated with more action to correct the negative situation.

The research of Harmon-Jones, Sigelman et al. (2003) supports the hypothesis

that the left frontal cortical region is involved in approach motivation rather than positive

affect. Moreover, the results suggest that the left frontal region is most accurately

described as a region sensitive to motivational intensity. That is, it was only when anger

was associated with an opportunity to behave in a manner to resolve the anger-producing

event that participants evidenced the increased relative left frontal activation.

Proneness toward Hypomania/Mania and Anger-Related Left Frontal Cortical Activity

The reviewed research suggests that anger is related to relative left frontal cortical

activity because anger is associated with approach motivation. Consequently, individuals

with greater trait approach motivation may be particularly likely to evidence greater left

frontal activity in response to an anger-provoking situation, as they feel motivated to

redress the anger-provoking situation. In contrast, individuals with lower trait approach

motivation may be particularly unlikely to evidence greater left frontal activity and may

instead respond with lower left frontal activity, as they feel hopeless to redress the anger-

provoking situation. To examine these ideas, Harmon-Jones, Abramson, Sigelman,

Bohlig, Hogan, and Harmon-Jones (2002) exposed individuals with high and low trait

approach motivation to an anger-producing situation. Based on the observed link between

hypomania/mania and increased approach motivation (Depue & Iacono, 1989; Meyer et

al., 1999), we predicted that proneness toward mania would be related to increased

relative left frontal activity in response to an anger-evoking event. In contrast, based on

the link between depression and decreased approach motivation (Depue & Iacono, 1989;


Fowles, 1993; Henriques & Davidson, 1990), we predicted that proneness toward

unipolar depression would be related to decreased relative left frontal activity in response

to the anger-invoking event. To assess these individual differences characteristics among

a sample of unselected undergraduate students, we used the General Behavior Inventory,

which was developed to identify individuals who are at risk for developing these

disorders (Depue & Klein, 1988; Depue, Krauss, Spoont, & Arbisi, 1989). Results

indicated that tendencies toward hypomania/mania related to increased left frontal

activity, and that tendencies toward unipolar depression related to decreased left frontal

activity following exposure to the anger-provoking radio editorial. In these analyses,

resting, baseline relative left frontal activity was statistically controlled, suggesting that

the effects were specific to when anger was aroused.

Sympathy Reduces Anger-Related Left Frontal Activity

Whereas the reviewed evidence links approach anger to relative left frontal

activity, it is important to establish that manipulations that reduce angry approach

behaviors also reduce relative left frontal activity. To address this issue, we tested

whether sympathy would reduce the relative left frontal activity typically observed during

anger. Past research has suggested that experiencing sympathy for another individual can

reduce aggression toward that individual (e.g., see review by Miller & Eisenberg, 1988).

We hypothesized that sympathy may reduce aggression by reducing the relative left

frontal activity associated with anger. To test this hypothesis, college students were told

that the study concerned personality, perception, and brain activity, and that they and

another student would be writing essays and evaluating each other based on the essays.

Participants then wrote a persuasive essay arguing either for or against a 10% tuition


increase. Then, the experimenter returned to the participants’ room and handed them a

folder containing a reading perspective, an essay, and a questionnaire.

The reading perspective instructions asked participants to remain completely

objective (low sympathy) or to try to imagine how the other person must feel (high

sympathy), as in much past sympathy research (Batson, 1991, 1998; Harmon-Jones,

Peterson, & Vaughn, 2003; Stotland, 1969). The participant then read the essay

ostensibly written by the other participant. In the essay, the other participant described

his/her difficulties with having Multiple Sclerosis.

Following the reading of the essay, the participant received an evaluation of

his/her essay ostensibly written by other participant. The evaluation contained either

neutral ratings and comments (no insult) or insulting ratings and comments (insult).

Immediately after feedback manipulation, EEG was collected. Then, the participant

completed questionnaires assessing impressions of the other participant and emotions.

Results indicated that the insult evoked greater left frontal activity but only when

high levels of sympathy were not first evoked for the insulting person. Additional

comparisons revealed that the high sympathy/insult condition produced greater relative

left frontal activity than every other condition. Thus, when participants first experienced

sympathy for the target person, they did not evidence increased left frontal activity when

insulted. The experiment thus suggested that the alteration of relative left frontal activity

via sympathy can reduce angry aggression.

Manipulation of Left Frontal Cortical Activity and Attentional Processing of Anger

In addition to the reviewed evidence, other research is consistent with the

hypothesis that anger is associated with left frontal activity. For example, d’Alfonso, van


Honk, Hermans, Postma, and de Haan (2000) recently used slow repetitive transcranial

magnetic stimulation (rTMS) to inhibit the left or right prefrontal cortex. They found that

rTMS applied to the right prefrontal cortex caused selective attention towards angry faces

whereas rTMS applied to the left prefrontal cortex caused selective attention away from

angry faces. Because slow rTMS produces inhibition of cortical excitability, these results

suggests that the rTMS applied to the right prefrontal cortex decreased its activation and

caused the left prefrontal cortex to become more active. The same holds true for the

rTMS applied to the right prefrontal cortex and activation of the left prefrontal cortex.

The increase in left prefrontal activity led participants to attentionally approach angry

faces, as in an aggressive confrontation. In contrast, the increase in right prefrontal

activity led participants to attentionally avoid angry faces, as in a frightening

confrontation. The interpretation of these results, which d’Alfonso et al. advanced,

concurs with other research that has demonstrated that attention toward angry faces is

associated with high levels of self-reported anger and that attention away from angry

faces is associated with high levels of cortisol (van Honk, Tuiten, de Haan, van den Hout,

& Stam, 2001; Van Honk, Tuiten, Van den Hout, Koppeschaar, Thijssen, & de Haan,

1998; van Honk, Tuiten, Verbaten, van den Hout, Koppeschaar, Thijssen, & de Haan,

1999), which is associated with fear.

Research on Anger Using Other Brain Imaging Methods

Whereas the above-reviewed research has revealed that the left frontal cortical

region is involved in approach motivation and anger, it is limited in that EEG is the sole

imaging method used. While EEG possesses excellent temporal resolution, its spatial

resolution is limited. A search of the literature revealed two experiments that had


examined the effects of anger on brain activity measured with brain imaging methods

other than EEG.1 Both experiments utilized positron emission tomography (PET). One

used oxygen-15-labeled carbon dioxide to study normalized regional cerebral blood flow

during anger as compared to a neutral control state (Dougherty et al., 1999). In the

experiment, eight healthy men provided a written description of a time when they were

the most angry they had been in their life. The neutral scripts were generated by the

experimenters (i.e., going for a walk, cooking dinner). Based on the anger material

provided by the participant and the experimenter-generated neutral information, the

experimenter created a script in the second person and then audiotaped it in a neutral

voice for playback in the lab. The scripts were 30-40 sec long. Other emotions were

activated in a similar manner but the results were not published in the report. Emotion

induction time was counterbalanced across participants. Before each scan, the participant

was told to close his eyes, listen to the script, and “imagine the event portrayed as vividly

as possible, as if he was actually participating in the event, rather than just ‘watching

himself’ in it.” (p. 467). Participants were asked to recall and imagine the event for 60 sec

following the script audiotape. Positron emission tomography (PET) data were collected

during this time period. The anger and neutral conditions did not differ on heart rate, skin

conductance, or frontalis muscle activity, even though past research would suggest that

differences between conditions should emerge (e.g., Jaencke, 1996; Lavoie, Miller,

Conway, & Fleet, 2001). Perhaps anger was not evoked or perhaps the anger was not

sufficiently strong to affect these variables. However, the anger condition reported

greater anger than the neutral condition. The PET results revealed that as compared to

neutral imagery, anger imagery caused an increase in the left orbital frontal cortex, the

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Lavoie-Kim-L+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Miller-Sydney-B+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Conway-Michael+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Fleet-Richard-P+in+AU


right anterior cingulate cortex, the bilateral anterior temporal poles, left precentral gyrus,

bilateral medial frontal cortex, and bilateral cerebellum. No significant differences

emerged between conditions in the amydala or insular cortex.

Thus, the increase in activity in the left orbital frontal cortex is consistent with the

anger research results obtained using EEG. However, Dougherty et al. (1999) interpreted

the increase in left orbital frontal cortical activity as corresponding “to inhibition of

aggressive behavior in the face of anger.” (p. 471). While this interpretation is consistent

with some speculations of the role of the left orbital frontal cortex in response inhibition

(Mega et al., 1997), it is inconsistent with the EEG results showing that increased left

frontal activity is associated with increased aggression and approach behavior (e.g.,

Harmon-Jones & Sigelman, 2001; Harmon-Jones et al., 2003). The interpretation that the

left frontal cortical region is involved in the inhibition of anger and aggression is also

inconsistent with lesion data suggesting that mania results from damage to the right

frontal region (e.g., Robinson & Downhill, 1995) and results obtained when the left

relative to right frontal cortex is activated and angry attentional processes are measured

(e.g., d’Alfonso et al., 2000). However, it is possible that the EEG is assessing

dorsolateral frontal cortical activity and not orbital frontal activity, and that left orbital

frontal activity is involved in the inhibition of anger, whereas left dorsalateral frontal

activity is involved in approach motivations like anger.

In another experiment (Kimbrell et al., 1999), using H2 15O PET, 18 healthy

participants were instructed to recall anxious, angry, or neutral events and then “recall the

emotion they felt during that time and to try to experience it that way again.” (p. 455).

Affect-congruent faces were displayed to participants during the recall “to help subjects


re-experience and sustain the emotion.” (p. 455). Compared to the neutral recall task, the

anger recall task evoked increased activity in the left superior temporal gyrus, left inferior

frontal cortex, right thalamus, and right posterior cingulate. Anger also evoked decreased

regional cerebral blood flow in the right superior temporal gyrus, inferior parietal cortex,

and right middle frontal gyrus. However, when anger and anxiety were compared, anger

was associated with greater activity in the brainstem, right medial frontal gyrus, and right

inferior frontal gyrus. Thus, these results suggest that while both anxiety and anger

caused increases in some areas of the left frontal region (as compared to neutral), anger

caused greater activations in some area of the right frontal cortex and brainstem activity

than anxiety. Based on research suggesting that retrieval of personally relevant, time-

specific memories activates the left temporal pole (Maguire et al., 1999), Kimbrell et al.

(1999) suggested “that the common activations by anxiety and anger in the left anterior

temporal and inferior frontal cortical area relate to the nonspecific aspects of recall of

negative emotion…” (p. 461). Clearly, the results of Kimbrell et al. (1999) are

inconsistent with the EEG results reviewed herein and the results of Dougherty et al.

(1999).

As Kimbrell et al. (1999) noted, there were a number of limitations to the

experiment, including the variety of past events recalled and whether the recall task

evoked the actual emotion (the same limitation apply to Dougherty et al., 1999).

Consistent with their concerns about comparing actual emotional experience to imagined

emotional experience, research has demonstrated that moving a thumb activates primary

motor cortex (Rao et al., 1995), whereas imagining moving a thumb activates

supplemental motor cortex (Parsons et al., 1995).


Of course, it may be difficult to compare anger induced by imagery to anger

induced by insulting feedback or goal blocking, as in Harmon-Jones and Sigelman (2001)

and Harmon-Jones, Sigelman et al. (2003). In the imagery experiments, there was no

report of a significant association between reported anger and regional brain activity. In

the EEG experiments using means other than imagery to induce anger, self-reported

anger has been found to correlate significantly with relative left frontal activity (Harmon-

Jones & Sigelman, 2001; Harmon-Jones, Sigelman et al., 2003). Examination of

correlations between reported emotion and physiological measures assists in determining

whether the brain activation is related to emotional experience or some other non-

emotional variable.

Comparisons of Violent to Non-Violent Individuals on Frontal Lobe Function

The results indicating that relatively greater left frontal cortical activity is

associated with increased approach-oriented anger and behavior are seemingly

inconsistent with evidence suggesting that violent individuals have reduced frontal lobe

function (e.g., Amen et al., 1996; Raine, Stoddard, Bihrle, & Buchsbaum, 1998; Raine,

Meloy et al., 1998). These results, and others, have led some to conclude that the

prefrontal cortex, particularly the left orbital frontal cortex (and frontal activations

derived from EEG), is involved in the regulation of negative affects like anger (Davidson,

Putnam, & Larson, 2000).

However, other research has more strongly implicated right frontal regions in

violence. For example, Raine, Stoddard et al. (1998) found that murderers who came

from relatively good home backgrounds showed reduced prefrontal functioning,

compared to murderers from relatively bad home backgrounds and normal controls. In


particular, the greatest reduction in prefrontal functioning was found in the right

orbitofrontal cortex. Raine, Park et al. (2001) provided further support for this

interpretation in a continuous performance task study that assessed fMRI in violent

offenders. Results indicated that violent offenders who had suffered severe child abuse

evidenced reduced right hemispheric functioning, particularly in the right temporal

cortex. In contrast, individuals who had suffered severe child abuse and had refrained

from violence evidenced relatively lower left but higher right activity in the temporal

lobe. These results suggest that the reduced right temporal activity coupled with severe

child abuse was associated with being violent.

These findings are consistent with the reviewed EEG research (Harmon-Jones &

Allen, 1998; Harmon-Jones et al., 2002; Harmon-Jones et al., 2003), which found that

approach-oriented anger was associated with reduced right frontal activity (in addition to

increased left frontal activity). Other research has revealed that increased activity in the

right frontal cortex is associated with withdrawal motivation. Perhaps the violent

individuals who showed reduced right frontal activity in the studies of Raine and

colleagues (1998, 2001) lack the behavioral constraints engendered by the withdrawal

motivation system that may be partially instantiated in the right frontal cortex.

However, other studies have implicated reduced activity in both left and right

frontal cortices in violence and aggression. For instance, Raine, Meloy et al. (1998) found

in a PET study that affective murderers, as compared to predatory murderers and normal

controls, evidenced reduced lateral and medial prefrontal activity in both hemispheres

during a continuous performance task.


Of course, differences in participant samples may explain the differences in

results. That is, most of the anger studies have involved normal individuals, whereas the

studies on violence have involved extremely violent individuals. However, in the

Harmon-Jones and Allen (1998) study, seven of the participants were adolescents who

were in an in-patient psychiatric unit for impulse control disorders. But even among this

sample, trait anger was related to greater left frontal activity and reduced right frontal

activity at rest. These results suggest that the samples may not be the source of the

differences. However, the Harmon-Jones and Allen (1998) samples was much younger

than samples used in other studies comparing frontal lobe function in violent and non-

violent individuals (e.g., Raine, Maloy et al., 1998). The longer lifetime of violence in

adults may cause the reductions in frontal cortical activity.

The studies comparing brain function of violent and non-violent individuals

typically assess frontal lobe function at rest or during a cognitive task and not during

anger-arousing situations. For example, Raine, Maloy et al. (1998) measured PET during

a continuous performance task. However, it is not clear that reduced frontal lobe function

measured during these tasks causes violence. The violent individuals (as compared to the

non-violent individuals) who display less prefrontal activity during cognitive tasks may

simply be less motivationally/emotionally engaged by the relatively unemotional nature

of the tasks. However, violent individuals may not demonstrate reduced frontal lobe

function during a more emotionally engaging situation, such as an interpersonal

provocation. It seems that the brain activation during such events would be more

predictive of violent behavior.


Another difficulty emerges when attempting to compare studies of violent

offenders with the studies on anger: anger can be manipulated in the lab, whereas being a

violent offender cannot be manipulated. Thus, in the latter type of studies, there are the

omnipresent difficulties associated with correlational studies. For instance, the violence

may have caused the reduction in frontal activity. Longitudinal studies are needed in

which brain function and violence are measured at several time points, starting in youth

and through adulthood. Such a design would allow researchers to more conclusively infer

whether brain function predicts violence.

In future research on the role of the frontal cortex in anger and violence, it will be

important to distinguish whether the effects of violence on prefrontal activity are due to

anger, impulsivity, or some other variable. In other words, do the causes of the violence

play an important role in the relationship of violence with prefrontal activity?

Importantly, the recent work by Raine and colleagues has begun this type of research as

they have examined differences between affective and predatory murderers, and how

socialization affects relationships between violence and prefrontal activity. Because the

left prefrontal region is supplied with a high density of serotonin type 2 receptors (e.g.,

Mann et al., 1996), and because serotonin has been found to relate to impulsivity (e.g.,

Soloff et al., 2000), it is possible that the reductions in prefrontal activity are due to

impulsivity and not necessarily anger and violence.

Conclusion

In sum, the reviewed experimental research suggests that increased activation of

the left frontal cortical region is associated with approach-oriented anger, whereas

decreased activation of the right frontal cortical region is associated with approach-


oriented anger. Evidence also suggests that this pattern of frontal cortical activation is

associated with approach behaviors, some of which can be destructive – aggression

against another person (Harmon-Jones & Sigelman, 2001), and some of which can be

constructive – action taken to resolve a perceived social injustice (Harmon-Jones,

Sigelman et al., 2003). Future research will benefit the understanding of anger by using

brain imaging methodologies with greater spatial resolution to examine neural correlates

of actual outbursts of anger that lead to constructive as well as destructive behaviors.

Moreover, examinations of the neural circuitry of non-violent and violent individuals

during outbursts of anger will assist in understanding one of society’s most destructive

emotions.


References

Ahern, G. L., & Schwartz, G. E. (1985). Differential lateralization for positive and

negative emotion in the human brain: EEG spectral analysis. Neuropsychologia,

23, 745-755.

Allen, J. J. B., Harmon-Jones, E., & Cavender, J. (2001). Manipulation of frontal EEG

asymmetry through biofeedback alters self-reported emotional responses and

facial EMG. Psychophysiology, 38, 685-693.

Amen, D.G., Stubblefield, M., Carmichael, B., & Thisted, R. (1996). Brain SPECT

findings and aggressiveness. Annals of Clinical Psychiatry, 8, 129 –137.

Baron, R. A. (1977). Effects of victim's pain cues, victim's race, and level of prior

instigation upon physical aggression. Journal of Applied Social Psychology, 9,

103-114.

Batson, C. D. (1991). The altruism question: Toward a social-psychological answer.

Hillsdale, NJ: Lawrence Erlbaum.

Batson, C. D. (1998). Altruism and prosocial behavior. In D. T. Gilbert, S. T. Fiske, & G.

Lindzey (Eds.), The handbook of social psychology (4th ed., Vol. 2, pp. 282-316).

Boston, MA: McGraw-Hill.

Berkowitz, L., Cochran, S., & Embree, M. (1981). Physical pain and the goal of

aversively stimulated aggression. Journal of Personality and Social Psychology,

40, 687-700.

Blanchard, D. C., & Blanchard, R. J. (1984). Affect and aggression: An animal model

applied to human behavior. Advances in the study of aggression, 1, 1-62.


Blanchard, D. C. & Takahashi, S. N. (1988). No change in intermale aggression after

amygdala lesions which reduce freezing. Physiology and Behavior, 42, 613-616.

Boissy, A., & Bouissou, M F. (1994). Effects of androgen treatment on behavioral and

physiological responses of heifers to fear-eliciting situations. Hormones and

Behavior, 28, 66-83.

Brehm, J. W., & Self, E. (1989). The intensity of motivation. In M. R. Rosenzweig, & L.

W. Porter, Annual Review of Psychology (Vol. 40, pp. 109-131). Palo Alto, CA,

USA: Annual Reviews, Inc.

Busch, D. E. & Barfield, R. J. (1974). A failure of amygdaloid lesions to alter agonistic

behavior in the laboratory rat. Physiology and Behavior, 12, 887-892.

Buss, A. H., & Perry, M. (1992). The aggression questionnaire. Journal of Personality

and Social Psychology, 63, 452-459.

Carver, C. S., and White, T. L. (1994). Behavioral inhibition, behavioral activation, and

affective responses to impending reward and punishment: The BIS/BAS scales.

Journal of Personality and Social Psychology, 67, 319-333.

Carver, C. S. (2001). Affect and the functional bases of behavior: On the dimensional

structure of affective experience. Personality and Social Psychology Review, 5,

345-356.

Cassidy, F., Forest, K., Murry, E., & Carroll, B. J. (1998). A factor analysis of the signs

and symptoms of mania. Archives of General Psychiatry, 55, 27-32.

Coan, J.A., & Allen, J.J.B. (2003). The state and trait nature of frontal EEG asymmetry in

emotion. In K. Hugdahl and R. J. Davidson (Eds.) The Asymmetrical Brain

(pp.565-615), Cambridge, MA: MIT Press.


Coan, J. A., Allen, J. J. B., & Harmon-Jones, E. (2001). Voluntary facial expression and

hemispheric asymmetry over the frontal cortex. Psychophysiology, 38, 912-925.

Cook, I. A., O’Hara, R., Uijtdehaage, S. H. J., Mandelkern, M., & Leuchter, A. F. (1998).

Assessing the accuracy of topographic EEG mapping for determining local brain

function. Electroencephalography and Clinical Neurophysiology, 107, 408-414.

d’Alfonso, A. A. L., van Honk, J., Hermans, E., Postma, A., & de Haan, E. H. F. (2000).

Laterality effects in selective attention to threat after repetitive transcranial

magnetic stimulation at the prefrontal cortex in female subjects. Neuroscience

Letters, 280, 195-198.

Darwin, C. (1872/1965). The expression of the emotions in man and animals. Chicago,

IL: The University of Chicago Press.

Davidson, R. J. (1998). Anterior electrophysiological asymmetries, emotion, and

depression: Conceptual and methodological conundrums. Psychophysiology, 35,

607-614.

Davidson, R. J., Chapman, J. P., Chapman, L. J., & Henriques, J. B. (1990).

Asymmetrical brain electrical activity discriminates between psychometrically-

matched verbal and spatial cognitive tasks. Psychophysiology, 27, 528-543.

Davidson, R. J., & Fox, N. A. (1982). Asymmetrical brain activity discriminates between

positive and negative affective stimuli in human infants. Science, 218, 1235-1236.

Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants' response

to maternal separation. Journal of Abnormal Psychology, 98, 127-131.


Davidson, R. J., Putnam, K. M., & Larson, C. L. (2000). Dysfunction in the neural

circuitry of emotion regulation – A possible prelude to violence. Science, 289,

591-594.

Depue, R. A. & Iacono, W. G. (1989). Neurobehavioral aspects of affective disorders.

Annual Review of Psychology, 40, 457-492.

Depue, R. A. & Klein, D. N. (1988). Identification of unipolar and bipolar affective

conditions in nonclinical and clinical populations by the General Behavior

Inventory. In (Eds.) D. L. Dunner, E. S. Gershon, and J. E. Barrett, Relatives at

risk for mental disorder (pp. 179 - 202). New York: Raven Press.

Depue, R. A., Krauss, S., Spoont, M. R., & Arbisi, P. (1989). General behavior inventory

identification of unipolar and bipolar affective conditions in a nonclinical

university population. Journal of Abnormal Psychology, 98, 117-126.

Dougherty, D. D., Shin, L. M., Alpert, N. M., Pitman, R. K., Orr, S. P., Lasko, M.,

Macklin, M. L., Fischman, A. J., & Rauch, S. L. (1999). Anger in health men: A

PET study using script-driven imagery. Biological Psychiatry, 46, 466-472.

Ekman, P., & Davidson, R. J. (1993). Voluntary smiling changes regional brain activity.

Psychological Science, 4, 342-345.

Flynn, J., Vanegas, H., Foote, W., & Edwards, S. B. (1970). Neural mechanisms involved

in a cat’s attack on a rat. In R. Whalen, R. F. Thompson, M. Verzeano, & N.

Weinberger (Eds.), The neural control of behavior (pp. 135-173). New York:

Academic Press.


Fowles, D. C. (1993). Behavioral variables in psychopathology: A psychobiological

perspective. In P. B. Sutker & H. E. Adams (Eds.), Comprehensive handbook of

psychopathology (2nd ed., pp. 57-82). New York: Plenum.

Fox, N. A. (1991). If it’s not left, it’s right. American Psychologist, 46, 863-872.

Gotlib, I. H., Ranganath, C., & Rosenfeld, J. P. (1998). Frontal EEG alpha asymmetry,

depression, and cognitive functioning. Cognition and Emotion, 12, 449-478.

Gray, J. A. (1994a). Personality dimensions and emotion systems. In P. Ekman & R. J. Davidson

(Eds.), The nature of emotion: Fundamental questions (pp. 329-331). New York: Oxford

University Press.

Gray, J. A. (1994b). Three fundamental emotion systems. In P. Ekman, & R. J. Davidson

(Eds.), The nature of emotion: Fundamental questions (pp. 243-247). New York:

Oxford University Press.

Harmon-Jones, E. (2000). The role of affect in cognitive dissonance processes. In J.

Forgas (Ed.), Handbook of affect and social cognition (pp. 237-255). Lawrence

Erlbaum.

Harmon-Jones, E. (in press-a). Anger and the behavioural approach system. Personality

and Individual Differences.

Harmon-Jones, E. (in press-b). On the relationship of anterior brain activity and anger:

Examining the role of attitude toward anger. Cognition and Emotion.

Harmon-Jones, E., Abramson, L. Y., Sigelman, J., Bohlig, A., Hogan, M. E., & Harmon-

Jones, C. (2002). Proneness to hypomania/mania or depression and asymmetrical

frontal cortical responses to an anger-evoking event. Journal of Personality and

Social Psychology, 82, 610-618.


Harmon-Jones, E., & Allen, J. J. B. (1997). Behavioral activation sensitivity and resting

frontal EEG asymmetry: Covariation of putative indicators related to risk for

mood disorders. Journal of Abnormal Psychology, 106, 159-163.

Harmon-Jones, E., & Allen, J. J. B. (1998). Anger and prefrontal brain activity: EEG

asymmetry consistent with approach motivation despite negative affective

valence. Journal of Personality and Social Psychology, 74, 1310-1316.

Harmon-Jones, E., Peterson, H., & Vaughn, K. (2003). The dissonance-inducing effects

of an inconsistency between experienced empathy and knowledge of past failures

to help: Support for the action-based model of dissonance. Basic and Applied


Harmon-Jones, E., & Sigelman, J. (2001). State anger and prefrontal brain activity:

Evidence that insult-related relative left prefrontal activation is associated with

experienced anger and aggression. Journal of Personality and Social Psychology,

80, 797-803.

Harmon-Jones, E., Sigelman, J. D., Bohlig, A., & Harmon-Jones, C. (2003). Anger,

coping, and frontal cortical activity: The effect of coping potential on anger-

induced left frontal activity. Cognition and Emotion, 17, 1-24.

Heller, W. (1990). The neuropsychology of emotion: Developmental patterns and

implications for psychopathology. In (Eds.), N. L. Stein, B. Leventhal, & T.

Trabasso, Psychological and biological approaches to emotion (pp. 167-211).

Hillsdale, New Jersey: Lawrence Erlbaum Associates.


Heller, W., & Nitschke, J. B. (1998). The puzzle of regional brain activity in depression

and anxiety: The importance of subtypes and comorbidity. Cognition and

Emotion, 12, 421-447.

Henriques, J. B., & Davidson, R. J. (1990). Regional brain electrical asymmetries

discriminate between previously depressed and healthy control subjects. Journal

of Abnormal Psychology, 99, 22-31.

Izard, C. E. (1991). The psychology of emotions. New York: Plenum Press.

Jacobs, G. D., & Snyder, D. (1996). Frontal brain asymmetry predicts affective style in

men. Behavioral Neuroscience, 110, 3-6.

Jaencke, L. (1996). Facial EMG in an anger-provoking situation: Individual differences

in directing anger outwards or inwards. International Journal of

Psychophysiology, 23, 207-214.

Kimbrell, T. A., George, M. S., Parekh, P. I., Ketter, T. A., Podell, D. M., Danielson, A.

L., Repella, J. D., Benson, B. E., Willis, M. W., Herscovitch, P., & Post, R. M.

(1999). Regional brain activity during transient self-induced anxiety and anger in

healthy adults. Biological Psychiatry, 46, 454-465.

Lagerspetz, K. M. J. (1969). Aggression and aggressiveness in laboratory mice. (In S.

Garattini & E. B. Sigg (Eds.), Aggressive behavior (pp. 77—85). New York:

Wiley.)

Lavoie, K. L., Miller, S. B., Conway, M., & Fleet, R. P. (2001). Anger, negative

emotions, and cardiovascular reactivity during interpersonal conflict in women.

Journal of Psychosomatic Research, 51, 503-512.

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Lavoie-Kim-L+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Miller-Sydney-B+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Conway-Michael+in+AU

http://webdbs.library.wisc.edu:8585/webspirs/doLS.ws?ss=Journal-of-Psychosomatic-Research+in+SO


Lazarus, R. S. (1991). Emotion and adaptation. New York: Oxford.

Lerner, J. S., & Keltner, D. (2001). Fear, anger, and risk. Journal of Personality and


Lewis, M., Sullivan, M. W., Ramsey, D. S., & Alessandri, S. M. (1992). Individual

differences in anger and sad expressions during extinction: Antecedents and

consequences. Infant Behavior and Development, 15, 443-452.

Maguire, E.A., & Mummery, C.J. (1999). Differential modulation of a common memory

retrieval network revealed by positron emission tomography. Hippocampus, 9,

54–61.

Malone, R. P., Delaney, M. A., Luebbert, J. F., Cater, J., & Campbell, M. (2000). A

double-blind placebo-controlled study of lithium in hospitalized aggressive

children and adolescents with conduct disorder. Archives of General Psychiatry,

57, 649-654.

Mann, J. J., Malone, K. M., Diehl, D. J., Perel, J., Cooper, T. B., Mintun, M. A. (1996).

Demonstration in vivo of reduced serotonin responsivity in the brain of untreated

depressed patients. American Journal of Psychiatry, 153, 174-182.

Mega M.S., Cummings J.L., Salloway S., & Malloy P. (1997). The limbic system: an

anatomic, phylogenetic, and clinical perspective. Journal of Neuropsychiatry and

Clinical Neuroscience, 9, 315–330.

Meyer, B., Johnson, S. L., & Carver, C. S. (1999). Exploring behavioral activation and

inhibition sensitivities among college students at risk for bipolar spectrum


symptomatology. Journal of Psychopathology and Behavioral Assessment, 21,

275-292.

Mikulincer, M. (1988). Reactance and helplessness following exposure to unsolvable

problems: The effects of attributional style. Journal of Personality and Social

Psychology, 54, 679-686.

Miller, P. A., & Eisenberg, N. (1988). The relation of empathy to aggressive and

externalizing/antisocial behavior. Psychological Bulletin, 103, 324-344.

Moyer, K. E. (1976). The psychobiology of aggression. New York: Harper & Row.

Oatley, K., & Jenkins, J. M. (1996). Understanding emotions. Oxford, England UK:

Blackwell Publishers, Inc.

Olweus, D. (1986). Aggression and hormones: Behavioral relationship with testosterone

and adrenaline. In D. Olweus, J. Block, & M. Radke-Yarrow (Eds.), Development

of antisocial and prosocial behavior: Research, theories, and issues (pp. 51 – 72).

Orlando: Academic Press.

Parsons, L.M., Fox, P.T., Downs, J.H., Glass, T., Hirsch, T.B., Martin, C.C. (1995). Use

of implicit motor imagery for visual shape discrimination as revealed by PET.

Nature 375:54 –58.

Plutchik, R. (1980). Emotion: A psychoevolutionary synthesis. New York: Harper and

Row.

Rao, S.M., Binder, J.R., Hammeke, T.A., Bandettini, P.A., Bobholz, J.A., Frost, J.A.

(1995). Somatotopic mapping of the human primary motor cortex with functional

magnetic resonance imaging. Neurology, 45, 919 –924.


Raine, A., Meloy, J. R., Bihrle, S., Stoddard, J., LaCasse, L., & Buchsbaum, M. S.

(1998). Reduced prefrontal and increased subcortical brain functioning assessed

using positron emission tomography in predatory and affective murderers.

Behavioral Sciences and the Law, 16, 319-332.

Raine, A., Park, S., Lencz, T., Bihrle, S., LaCasse, L., Widom, C. S., Dayeh, L. A.,

Singh, M. (2001). Reduced right hemisphere activation in severely abused violent

offenders during a working memory task: An fMRI study. Aggressive Behavior,

27, 111-129.

Raine, A., Stoddard, J., Bihrle, S., & Buchsbaum, M. (1998). Prefrontal glucose deficits

in murderers lacking psychosocial deprivation. Neuropsychiatry,

Neuropsychology, and Behavioral Neurology, 11, 1-7.

Robinson, R. G., & Downhill, J. E. (1995). Lateralization of psychopathology in response

to focal brain injury. In R. J. Davidson & K. Hugdahl (Eds.), Brain Asymmetry

(pp. 693-711). Cambridge, MA: Massachusetts Institute of Technology.

Silberman, E. K., & Weingartner, H. (1986). Hemispheric lateralization of functions

related to emotion. Brain and Cognition, 5, 322-353.

Schaffer, C. E., Davidson, R. J., & Saron, C. (1983). Frontal and parietal

electroencephalogram asymmetry in depressed and nondepressed subjects.

Biological Psychiatry, 18, 753-762.

Soloff, P. H., Meltzer, C. C.,. Greer, P. J., Constantine, D., &. Kelly, T. M. (2000). A

fenfluramine-activated FDG-PET study of Borderline Personality Disorder.

Biological Psychiatry, 47, 540–547.


Stotland, E. (1969). Exploratory studies of empathy. In L. Berkowitz (Ed.), Advances in

experimental social psychology (Vol. 4, pp. 271-313). New York: Academic

Press.

Sutton, S. K., & Davidson, R. J. (1997). Prefrontal brain asymmetry: A biological

substrate of the behavioral approach and inhibition systems. Psychological

Science, 8, 204-210.

Tomarken A. J., Davidson R. J., Henriques J. B. (1990). Resting frontal brain asymmetry

predicts affective responses to films. Journal of Personality and Social

Psychology, 59, 791-801.

Tomarken, A. J., Davidson, R. J., Wheeler, R. E., & Doss, R. (1992). Individual

differences in anterior brain asymmetry and fundamental dimensions of emotion.

Journal of Personality and Social Psychology, 62, 676-687.

Tomarken, A. J., & Keener, A. D. (1998). Frontal brain asymmetry and depression: A

self-regulatory perspective. Cognition and Emotion, 12, 387-420.

Tyrer, S., & Shopsin, B. (1982). Symptoms and assessment of mania. In E. S. Paykel

(Ed.), Handbook of affective disorders (pp. 12-23). New York: Guilford Press.

Vandenheede, M., & Bouissou, M. F. (1993). Effect of androgen treatment on fear

reactions in ewes. Hormones and Behavior, 27, 435-448.

van Honk, J., Tuiten, A., de Haan, E., van den Hout, M., & Stam, H. (2001). Attentional

biases for angry faces: Relationships to trait anger and anxiety. Cognition and

Emotion, 15, 279-297.


van Honk, J., Tuiten, A., van den Hout, M., Koppeschaar, H., Thijssen, J., de Haan, E., &

Verbaten, R. (1998). Baseline salivary cortisol levels and preconscious selective

attention for threat: A pilot study. Psychoneuroendocrinology, 23, 741-747.

van Honk, J., Tuiten, A., Verbaten, R., van den Hout, M., Koppeschaar, H., Thijssen, J.,

& de Haan, E. (1999). Correlations among salivary testosterone, mood, and

selective attention to threat in humans. Hormones and Behavior, 36, 17-24.

Watson, D. (2000). Mood and temperament. New York: Guilford Press.

Wheeler, R. E., Davidson, R. J., & Tomarken, A. J. (1993). Frontal brain asymmetry and

emotional reactivity: A biological substrate of affective style. Psychophysiology,

30, 82-89.

Wortman, C. B., & Brehm, J. W. (1975). Responses to uncontrollable outcomes: An

integration of reactance theory and the learned helplessness model. In L.

Berkowitz (Ed.), Advances in Experimental Social Psychology (Vol. 8., pp. 278-

336). New York: Academic Press.

Young, P. T. (1943). Emotion in man and animal: Its nature and relation to attitude and

motive. New York: John Wiley and Sons.

Zajonc, R. B., & McIntosh, D. N. (1992). Emotions research: Some promising questions

and some questionable promises. Psychological Science, 3, 70-74.


Footnotes

1. While there have been several studies examining neural responses to photographs of

angry faces, there have only been a very few studies examining neural activity associated

with the experience or expression of anger. Because the former type of studies are likely

assessing neural processes associated with the perception of emotional stimuli and not

necessarily the experience or expression of emotion, these studies are not reviewed.

anger and aggression: human functional neuroimaging and...

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